Journal of Experimental Marine Biology and Ecology 348 (2007) 162 – 173
                                                       www.elsevier.com/locate/jembe




      The effects of temperature on producers, consumers, and
      plant–herbivore interactions in an intertidal community
                Bionda Morelissen a,1 , Christopher D.G. Harley b,c,⁎
             a
               Wageningen University, Department of Aquatic Ecology and Water Quality Management,
                      P.O. Box 8080, NL-6700 DD Wageningen, The Netherlands
                      b
                       Bodega Marine Laboratory, Bodega Bay, CA, 94923, USA
             c
               University of British Columbia, Department of Zoology, Vancouver, BC, Canada V6T1Z4
             Received 18 August 2006; received in revised form 25 April 2007; accepted 25 April 2007




Abstract

  Although global warming is acknowledged as a primary threat to populations and communities, the impact of rising temperature
on community structure remains poorly understood. In this study, we investigated the direct and indirect effects of temperature on
epilithic primary producers (micro- and macroalgae) and an abundant consumer, the rough limpet Lottia scabra, in the rocky
intertidal zone in central and northern California, USA. We factorially manipulated temperature and limpet abundance in the field
to determine the effects of temperature on herbivore growth and mortality, algal abundance, and the strength of plant–herbivore
interactions. Microalgal growth was positively affected by shading at both locations, and negatively affected by limpet grazing at
Pacific Grove but not at Bodega Bay. Macroalgae were only abundant at Bodega Bay, where changes in abundance were negatively
related to grazing and independent of temperature. Despite temperature-related changes in microalgal food supply, there were no
direct or indirect effects of temperature manipulation on L. scabra growth or mortality. Furthermore, temperature did not alter the
importance of herbivory at either site. These results indicate that the influence of increasing temperature, as is predicted with
climate change, will have differential effects on producers and consumers. However, thermal effects at one trophic level do not
necessarily propagate through the food web to other trophic levels.
© 2007 Elsevier B.V. All rights reserved.

Keywords: Herbivory; Lottia (Collisella) scabra; Macroalgae; Microalgae; Thermal stress; Top-down vs. bottom-up effects




1. Introduction                              coastal platforms may be up to 2.1 °C higher than at
                                      present (Hiscock et al., 2004; IPCC, 2001). Sea surface
  It has been widely recognized that global tempera-           temperatures may be up to 2.5 °C higher than in 2000
tures are rising (IPCC, 2001). It is predicted that by the         (Hiscock et al., 2004). However, because the ecological
2050s, average air temperatures relevant to rocky             impacts of climate change can depend on interactions
                                      among species (e.g. Sanford, 1999), the ecological
⁎ Corresponding author. University of British Columbia, Department    consequences of climatic warming are still largely
of Zoology, 6270 University Blvd., Vancouver, BC, Canada V6T1Z4.      unclear. In marine systems, one major challenge lies in
Tel.: +1 604 827 3431.
  E-mail address: harley@zoology.ubc.ca (C.D.G. Harley).
                                      understanding how interactions among species will
1
  Present address: Victoria University of Wellington, School of     ameliorate or enhance the effects of temperature change
Biological Sciences, PO Box 600, Wellington 6140, New Zealand.       (Harley et al., 2006).
0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2007.04.006
        B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173     163


  Rocky intertidal environments are extremely physi-       of thermal stress on high-intertidal micro- and macro-
ologically stressful habitats; temperatures can fluctuate      algae, grazing limpets, and plant–herbivore interactions.
swiftly and can reach lethal extremes during low tide        We hypothesized that increased thermal stress would
(Hiscock et al., 2004; Helmuth and Hofmann, 2001).         reduce limpet growth and increase limpet mortality. We
Because many intertidal organisms already live very         further hypothesized that thermal stress would reduce
close to their thermal tolerance limits (Somero, 2002),       microalgal biomass, but that this reduction would be
temperature has an important and pervasive influence on       partially or fully offset by reduced grazing rates.
the distribution and abundance of organisms via its
effects on physiological processes (Dahlhoff et al.,        2. Materials and methods
2001; Somero, 2002). Organisms living in the rocky
intertidal zone are therefore considered to be good         2.1. Study sites and organisms
indicators of climate change impacts (Helmuth and
Hofmann, 2001; Helmuth et al., 2002). Predicting            Experiments were conducted during the spring and
ecological responses to climate change, however,          summer of 2005 at two different locations along the
requires information on how abiotic changes are           coast of California, USA (Fig. 1): the Bodega Marine
mediated by interspecific interactions. For example,        Laboratory in Bodega Bay (38° 20′N, 123° 4′W), and
thermal conditions influence the importance of biolog-       the Hopkins Marine Station in Pacific Grove (36° 37′N,
ical interactions such as predation, competition, and        121° 54′W). The Californian rocky intertidal zone is
facilitation (Sanford, 1999; Leonard, 2000). To date,        ideal for addressing questions regarding thermal stress
studies which simultaneously manipulate abiotic and         and species interactions. Air temperatures are expected
biological variables remain rare.                  to rise in California, but sea surface temperatures may
  Biological communities are structured by both top-       not, due to steady or enhanced upwelling (see Bakun,
down and bottom-up processes (e.g., Nielsen, 2001),         1990). Therefore, examination of thermal stress at low
and temperature may influence both of these processes        tide is realistic in terms of expected future changes in the
(Thompson et al., 2004). For example, the abundance of       environment.
intertidal microflora depends on herbivory, local            The intertidal substratum at both study sites is
variation in light and temperature, and seasonal changes      granite, and both locations are wave exposed, although
in environmental conditions (Nicotri, 1977; Cubit,         some sites at each location are protected to varying
1984). Specifically, environmental conditions during        degrees by the peculiarities of the topography. The tides
the winter are sufficiently benign to allow microalgal       in the region are mixed semi-diurnal, with two unequal
production to outpace consumption (Cubit, 1984).          high and two unequal low tides each day. During March,
Temperature is also known to affect macroalgae (e.g.,        April, and May, lower low tides occur during the middle
Allison, 2004; Keser et al., 2005), and the combined        of the day and may be associated with high thermal
influence of temperature and herbivory can determine        stress for intertidal organisms at both locations (Suther-
the distribution and abundance of macroalgae via          land, 1970; Helmuth et al., 2002). From June through
disproportionately strong impacts on that trophic level       September, the lower low tides shift to the early morning
(Harley, 2003). Taken together, these results suggest that     hours, reducing the likelihood of thermal stress during
rising temperatures and associated physiological stress       low tide. In addition, coastal fog is common during the
can decrease primary and secondary production and          summer months, further ameliorating thermal stress.
alter the relative importance of herbivory.             However, occasional calm, sunny days may result in
  In this study we simultaneously investigated the        physiological stress at either location at any time during
effects of temperature and an abundant consumer, the        the spring and summer (e.g., Wolcott, 1973). Mean daily
rough limpet Lottia scabra (Gould) (formerly Collisella       maximum air temperatures during the spring and
scabra and Macclintockia scabra; see Gilman, 2007 for        summer typically range from 16 to 21 °C at the Bodega
the most recent treatment of the taxonomy of this          Marine Laboratory (Wolcott, 1973; Bodega Ocean
species) on community dynamics in the rocky intertidal       Observing Node dataset), and from 20 to 24 °C at the
zone in California, USA. Temperature was manipulated        Hopkins Marine Station (M. Denny; unpublished data).
with experimental shades. Limpet enclosures and             Bodega Bay has a fairly high biodiversity in the high
exclosures were used to investigate the effect of limpets      rocky intertidal. Mobile gastropods are abundant, and
on their algal food source in different temperature         include limpets (mainly L. scabra and L. digitalis),
treatments (shaded and non-shaded treatments). The         littorine snails (predominantly Littorina plena, but also
main focus of this research was to determine the effect       Littorina keenae and L. scutulata) and black turban
164        B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173




Fig. 1. Map of California with the locations of the two research sites: Bodega Bay and Pacific Grove. The top-left inserted map shows the Bodega Bay
research site at the Bodega Marine Reserve, with the locations of the 8 experimental sites. The research site in Pacific Grove, at the Hopkins Marine
Station, Stanford University, is shown in the bottom left insertion (adjusted map from Sagarin et al., 1999), along with the locations of the 6
experimental sites.



snails (Tegula funebralis). There is also a diverse              L. scabra is a generalist grazer, feeding on epilithic
macroalgal assemblage featuring Porphyra perforata,              microalgal film (Sutherland, 1970; Branch, 1981).
Mastocarpus papillatus, Endocladia muricata, and               L. scabra populations are known to be vulnerable to
Pelvetiopsis limitata as the most abundant species.              thermal stress: a mass mortality event was observed at
L. scabra is also abundant in high-intertidal communi-            Bodega Bay in the spring of 1967 when consecutive hot
ties in Pacific Grove. However, Pacific Grove differs             days coincided with late morning low tides (Sutherland,
from Bodega Bay in that it has a higher abundance of the           1970). Another thermally-mediated mortality event
owl limpet Lottia gigantea in the high-intertidal zone            reduced L. scabra populations at Bodega Bay in the
and a much greater abundance of L. keenae in the splash            spring of 2004 (Harley, unpubl. data). This encouraged
zone. Unlike Bodega Bay, there is very little macroalgae           us to investigate the possible effects of thermal stress on
in areas occupied by L. scabra in Pacific Grove.               this abundant consumer with regard to potential future
  In this study, we focused on the impacts of                climate change.
temperature on communities dominated by the limpet
L. scabra. L. scabra occupies shore levels from the              2.2. Field experiments
mid-intertidal zone to the splash zone (Sutherland,
1972; Haven, 1973; Sept, 2002). Larger (adult) animals              At Bodega Bay, experiments were initiated in March,
are most abundant in or just above the uppermost zone             2005. A total of eight experimental sites were selected in
of macroalgae on rocky shores (Sutherland, 1972;               areas where L. scabra were abundant. Six of the sites
Gilman, 2005). The snail shows homing behavior,                were situated within a south-west facing cove, with five
returning to its home scar nearly every low tide (Jessee,           sites on the south side and one site on the north side. The
1968; Connor and Quinn, 1984; Sommer, 1982).                 remaining two sites were on fully exposed, south-west
        B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173    165


facing benches (Fig. 1; top left insertion). Selection of      lacking vexar) were not attempted because mesh cages
sites ensured within-site similarity of substratum         and other “shade controls” can also have a considerable
orientation and limpet abundance, yet allowed for          effect on substrate temperature (Hayworth and Quinn,
among-site differences in substratum orientation. The        1990; Harley and Lopez, 2003).
intertidal height of the selected sites varied from 1.92 m       We placed iButton® temperature loggers (Dallas
to 2.70 m (mean ± standard deviation: 2.21 m ± 0.26 m)       Semiconductor, Dallas, Texas, USA) next to every
above Mean Lower Low Water. Plots within sites were         shaded and non-shaded fenceless control plot (i.e. a total
within 39 vertical cm of one another. Experiments in        of two loggers per block) to keep the record of the rock
Pacific Grove were initiated in April, 2005. At that        temperature (shaded or non-shaded) over time. Loggers
location only six sites were established. Again, sites       were placed immediately adjacent to the plots, such that
were selected for high L. scabra abundance and           they did not interfere with the experimental area yet
consistent within-site substrate orientation. The sites at     were still covered by the shade structure in shaded plots.
Pacific Grove ranged from 1.78 m to 3.08 m (2.43 ± 0.52)      To be able to place them, we chiseled off enough rock to
above MLLW. Plots within sites were within 27 vertical       create a small depression and used Epoxy putty (Sea
cm of one another.                         Goin' Poxy Putty, Heavy Duty; Permalite Plastics
  At each site within each of the two locations, six       Corporation, Costa Mesa, California, USA) to both
15 × 15 cm plots were selected. This plot size was         attach and completely cover the loggers. The tempera-
chosen according to the limpets' foraging behavior,         ture loggers were wrapped in parafilm before insertion
which is generally confined to within 10 cm of           into the epoxy putty for protection and easier removal of
individual home scars (Sutherland, 1970). In four of        the loggers at the end of the experiment. To mimic the
those plots, cages (15 × 15 cm, 3 cm tall; constructed out     surface albedo of the surrounding rock, fine dark beach
of 6 × 6 mm stainless steel wire mesh) were placed by        sand was pressed into the setting epoxy (Harley and
drilling holes into the rocky substratum, and using wall      Helmuth, 2003). The body temperature of a limpet is
anchors, stainless steel washers, and screw bolts to        very similar to the temperature of the rock upon which it
attach the cage to the rock. Two of the plots were left       sits; the latter is thus an excellent proxy for the former
without caging, but were marked 15 × 15 cm with screw        (Wolcott, 1973; Denny and Harley, 2006). The iButtons
bolts or Z-spar Epoxy Putty (A-788 Splash Zone           recorded temperature at 60-minute intervals from the
Compound; Z-spar Los Angeles, CA, USA) and used           end of March through the end of July 2005 at Bodega
as controls. Z-spar Epoxy Putty was also used to close       Bay and from the end of April through the end of July at
off the corners of cages when they could not be attached      Pacific Grove.
tightly to the rock by the bolts.                    At every site, limpet exclusion treatments were
  The plots at every site were assigned to two different     assigned to two of the caged plots (a shaded and a
temperature treatments: two caged plots and one open        non-shaded plot, randomly chosen), which were then
plot received no shading, the other two caged plots and       cleared of limpets and other grazers. In the remaining
open plot were shaded. The shades were made of heavy-        plots, there were an average of 9.7 ± 0.8 (mean ±standard
duty Vexar™ mesh (opening size 6 × 6 mm) strapped to        error) L. scabra per plot at Bodega Bay (excluding site
a PVC-coated galvanized steel welded cloth (opening         #7; see below), and 11.6 ± 0.8 L. scabra per plot at
size 25 × 25 mm) with cable ties. The shades were          Pacific Grove. Initial limpet densities did not vary
attached to the rock by means of stainless steel screw       among treatments (p N 0.3 in all cases). All the limpets
eyes anchored into the rock with wall anchors and cable       in the non-exclusion plots were tagged (only at Bodega
ties. Shades were open on two sides, and the “roof” was       Bay), using small numbered adhesive tags and glue
∼ 7 cm above the substratum. To minimize the            (Super Glue, liquid; Loctite, Dist. By Henkel Consumer
hydrodynamic influences, shades were placed in such         Adhesives, Inc., Avon, Ohio, USA) for identification
way that the waves surged parallel to the shade's two        purposes, and their shell size was measured with a pair
walls (i.e. water surged directly through the open sides      of dividers, the gape of which was measured with digital
rather than through the walled sides, see Harley, 2002).      calipers. This was done at the start and at the end of the
Similar shades reduced light levels by 60–65%,           experiment to determine individual growth over the
depending on ambient conditions (Harley, 2002). Our         four-month period. Other grazers (if present) were
experiments were conducted in spring and summer           removed from the plots, except from the “open” control
when irradiance was expected to be high enough to          plots.
prevent light limitation (see, e.g., Rasmussen et al.,         Microalgal biomass in the plots was estimated by
1983). Procedural controls for shading (e.g. wire mesh       measuring benthic chlorophyll a. Preliminary analyses
166       B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173


indicated that rock chips were a poor proxy for benthic         Bay, additional photos were taken at the mid-way point
chlorophyll because the rock tended to crumble and it          of the experiment. At the end of the experiment, limpet
was difficult to measure the true surface area of a           lengths were measured again to determine growth over
sample. Therefore, we used 1 × 1 cm ceramic tiles            the four-month period. Time limitations prevented us
(Mosaic Basics, Atlanta, GA), which eliminated any a           from tagging limpets in Pacific Grove; hence, limpet
priori spatial variation in benthic chlorophyll and           growth was not measured at that site. Limpet mortality/
provided an easily quantified surface for microalgal           absence and limpet recruitment were also recorded.
growth. Two replicate tiles were placed in the center of         Macroalgal percentage cover was determined in the field
every plot with the unglazed side facing up. The             and from photos at the start, middle and end of the
unglazed surface was roughened with coarse sand-paper          experiment in Bodega Bay, and at the start and end of
prior to deployment to better mimic the rock surface and         the experiment in Pacific Grove. Because macroalgal
create more favorable conditions for microalgal settle-         species composition was highly variable among blocks,
ment. The tiles were attached to the rocky substrate           analyses of individual macroalgal species were uninfor-
using Sea Goin' Poxy Putty (Heavy duty), to estimate           mative due to limited power. Therefore, we present
microalgal biomass/development inside the plots. Sea           analyses of total macroalgal cover.
Goin' Poxy Putty is nontoxic after it has set and is
readily colonized by invertebrates and algae (Harley,          2.3. Statistics
2002). At the end of the experiment the tiles were
removed and taken back to the laboratory to determine            Data were analyzed using JMP 5.1 (SAS institute).
the chlorophyll a content on the tiles. Every tile was put        Prior to statistical analysis, chlorophyll a data were log
into an individual test tube with 10 mL 90% HPLC             transformed and proportional limpet mortality data were
acetone. All samples were then vortexed and stored in          arcsine square-root transformed to meet the assumption
the freezer (− 4 °C) in the dark for 24 h. After this          of normality. Site number 7 at Bodega Bay was not
(passive) extraction time, samples were vortexed again          included in limpet growth and survival analyses because
and centrifuged for 5 min (6000 rpm) and then measured          this site contained only small individuals which were
by means of a fluorometer (TD-700, Tuner Designs)            impossible to tag individually. To determine macroalgal
using the method of Welschmeyer (1994). The two             responses to experimental treatments, we used change in
measurements from every plot were averaged to obtain a          percent cover as a response metric. The raw data
single estimate of chlorophyll a per plot.                conformed to the assumptions of an ANOVA during the
  Digital photos were taken of all the plots at the start        second half of the experiment (May–July), but not
and end of the experiment to determine changes in            during the first half. No transformation was able to
grazing activity/algal abundance, behavioral changes           remedy this problem. Thus, macroalgal results (based on
(change of home scars, migration), mortality, and            untransformed data) from April–late May should be
recruitment, besides observations in the field. In Bodega        interpreted with caution.




Fig. 2. A: Daily maximum rock temperature in the non-shaded treatments at Bodega Bay (mean of eight loggers) and Pacific Grove (mean of five
loggers) during spring/summer 2005.
         B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173           167


3. Results

3.1. Temperature

  The spring and summer of 2005 had no distinct heat
waves or extremely hot days (Fig. 2). Instead, it was
foggy for most of the experimental period. Owing to
temperature logger failures at Pacific Grove, only four
shaded and five non-shaded thermal time series were
usable.
  To investigate location and shade effects on substra-
tum temperature, we collapsed the time series for each
temperature logger into an average daily maximum
value (literally the mean of all daily maxima within a
given thermal time series) and performed statistical
analyses on those metadata. During the time that loggers
were deployed at both sites (30 April–21 July, 2005),
the effect of shading on average daily maximum
temperatures was highly significant (2-way ANOVA,
shade effect F1,21 = 30.1, p b 0.001), with shaded plots
remaining several degrees cooler than unshaded plots
(Fig. 3). The effect of location (Bodega Bay vs. Pacific
Grove), and the shading × location interaction, had no
significant effect on substratum temperature (2-way
ANOVA, location effect F1,21 = 0.01, p = 0.942; shadin-
g × location interaction F1,21 = 2.52, p = 0.127). Although
the interaction term was not significant, shades at           Fig. 4. The chlorophyll a content on tiles in the experimental plots at
Bodega Bay lowered rock temperatures slightly more           (A) Bodega Bay and (B) Pacific Grove. The effect of shading is
                                    significant at both locations, and the effect of limpet grazing is
                                    significant at Pacific Grove. Note that the significant main effects at
                                    Pacific Grove are obscured in this graph by the highly significant block
                                    effect (see Table 1 for details). Enclosure with limpets, no other
                                    grazers; Exclosure without any grazers; Control: open plots, with
                                    limpets and possibly other grazers (not fenced). Error bars are standard
                                    errors.


                                    than at Pacific Grove (∼ 5.9 °C vs. ∼ 3.3 °C, res-
                                    pectively). By comparison, Harley and Lopez (2003)
                                    showed a difference of 4 °C in earlier research with a
                                    similar shade design.

                                    3.2. Chlorophyll a

                                      In Bodega Bay, there was a strong effect of shading
                                    on chlorophyll a content (Fig. 4, Table 1); shaded plots
                                    had a higher chlorophyll a content than non-shaded
                                    plots. Neither limpets nor the limpet × shading interac-
                                    tion had any effect on the chlorophyll a content on the
Fig. 3. Average daily maximum rock temperature over the course of    substratum (Table 1). In Pacific Grove, by contrast, there
the experiment. Daily maximum temperature data were averaged      were effects of limpets, shading, and block (site) on
within each time series, and means and standard errors were generated
using these averages (N = 8 time series for Bodega Bay shaded and
                                    benthic chlorophyll a (Fig. 4, Table 1). In experimental
unshaded, N = 4 for Pacific Grove unshaded, and N = 5 for Pacific    plots in which limpets were present, the chlorophyll a
Grove shaded). See text for statistical analyses.            content on the ceramic tiles was lower than in plots in
168        B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173


Table 1                                   3.3. Macroalgal cover
Results of two-factor ANOVA (shade and limpet presence) on
chlorophyll a content at Bodega Bay and Pacific Grove
                                        The cover of macroalgal species in Bodega Bay was
Effect       Bodega Bay           Pacific Grove      low and variable among plots (means ± standard devia-
          df  F     p       df  F     p    tion during the May sampling: Porphyra sp. 5.1 ± 10.2,
Shade        1  54.6   b0.001     1  9.86    0.004  M. papillatus 3.9 ± 5.3, P. limitata 1.1 ± 2.9, all others
Limpets       2   0.01   0.991     2  6.31    0.006  b 1% cover). Therefore, macroalgal cover was analyzed
Shade × limpets   2   1.92   0.161     2  0.39    0.684  in aggregate. Macroalgal percent cover generally
Block        7   1.89   0.102     5  27.0    b0.001
                                      increased over the course of the experiment, particularly
Error        35               25
                                      in the limpet exclusion plots (Fig. 5). During the first
Significant effects (p b 0.05) in boldface type.              half of the experiment, the increase of macroalgal cover
                                      was weakly but significantly related to limpet abun-
                                      dance, with larger macroalgal increases in limpet
which limpets were excluded. Furthermore, as we               exclosures. There was no significant effect of shading
observed in Bodega Bay, the shaded plots in Pacific             or of the limpet × shade interaction (Table 2). However,
Grove contained more chlorophyll a than the non-              because the assumption of normality could not be met
shaded plots. Finally, the strong block effect indicates          during this time period, these results must be interpreted
that the location and orientation of the experimental sites         cautiously. During the second half of the experiment in
influenced the chlorophyll content in the plots.              Bodega Bay, increases in macroalgal cover continued to
                                      be highest in limpet exclosures, and the limpet effect
                                      was again significant (Table 2) despite the loss of
                                      macroalgal data from half of the unshaded inclusion and
                                      exclusion plots due to a procedural error. The blocking
                                      factor (site) was also significant at both sampling dates.
                                      Macroalgae were extremely rare in experimental plots in
                                      Pacific Grove, precluding formal analyses.
                                        In Bodega Bay, we found no relationship (facilitation
                                      or inhibition) between microalgal chlorophyll (log
                                      transformed) at the end of the experiment and macro-
                                      algal cover in May (linear regression: F1,46 = 1.71;
                                      p = 0.198) or macroalgal cover at the end of the
                                      experiment (linear regression: F1,38 = 3.13; p = 0.085;
                                      note the loss of 8 plots). Furthermore, macroalgal cover
                                      at either time point was not a significant covariate when


                                      Table 2
                                      Results two-factor ANOVA (shade and limpet presence) on changes in
                                      macroalgal percent cover during the first and second halves of the
                                      experiment at Bodega Bay
                                      Effect        Cover change        Cover change
                                                 (April–May)         (May–July)
                                                 df   F     p     df   F    p
                                      Shade         1   0.12   0.733    1   0.01   0.932
                                      Limpets        2   3.48   0.042    2   4.88   0.023
                                      Shade × limpets    2   0.08   0.920    2   0.60   0.559
                                      Block         7   3.18   0.010    3   3.45   0.044
                                      Error        35             15
                                      Significant effects (p b 0.05) in boldface type. Note that the assumption
Fig. 5. Change in macroalgal percent cover at Bodega Bay during the     of normality was violated in the April–May interval; thus, the results
first and second halves of the experiment (April–May and May–July,     from that time period should be interpreted with caution. Data from
respectively). Labels as in Fig. 4. Error bars are standard errors. See   four blocks were lost during the May–July time period; thus, the
Table 2 for statistical analyses.                      statistical analysis was conducted on the remaining four blocks.
          B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173     169


Table 3                                 (F1,25 = 7.0605; R2adj. = 0.388; p = 0.0135) influenced
Results of two-factor ANCOVA on limpet growth at Bodega Bay       average growth of the limpets in each plot. Small limpets
Effect                df    F       p     grew significantly faster than larger conspecifics, and
Shade                 1    0.0093     0.9240   those found lower on the shore grew faster than those
Fence                 1    4.2307     0.0517   found higher on the shore. When we included ‘Intertidal
Shade × fence             1    1.2093     0.2834   Height’ and ‘Average Initial Limpet Length’ as covari-
Intertidal height           1    7.7644     0.0108
                                     ates, we found that both influenced limpet growth, even
Average initial limpet length     1    6.8946     0.0154
Error                22                 after accounting for shading, limpet manipulation (fenced
                                     enclosures vs. unfenced controls), and the interaction term
The “fence” effect refers to fenced vs. unfenced (control) plots.
Intertidal height and average initial limpet length are treated as    (Table 3). None of the latter variables were significant
covariates in the analysis. Significant effects (p b 0.05) in boldface  (Table 3). There was also no direct relationship between
type.                                  substratum temperature and limpet growth, even after
                                     accounting for initial limpet length (p N 0.8).
included in an exploratory, full factorial analysis of           To further investigate potential bottom-up effects on
chlorophyll a (p N 0.05, full results not shown).            limpet growth at Bodega Bay, we compared limpet
                                     growth in enclosures to benthic chlorophyll in exclo-
3.4. Limpet mortality                          sures. There was no significant relationship between the
                                     two variables (ANCOVA, shade effect F = 0.13,
  The total number of limpets in experimental plots in         p = 0.728; chlorophyll effect F = 1.22, p = 0.293). When
Bodega Bay at the start of the experiment was 208            the non-significant shade term was dropped from the
(roughly 7.4 per non-exclusion plot in the seven blocks         analysis, there was still no relationship between benthic
where limpet abundance was tracked). At the end of the          chlorophyll and limpet growth (linear regression,
experiment this number had decreased by 14.9% to 177.          N = 14, F = 2.79, p = 0.121). Similar analyses between
In Pacific Grove, the total number of limpets at the start        limpet growth and macroalgal productivity (i.e. change
of the experiment was 279 (roughly 11.6 per non-             in macroalgal cover from April through late May) were
exclusion plot). At the end 242 limpets were still present        also non-significant (p N 0.1 in all cases).
(a 13.3% decrease). Because we cannot distinguish
mortality from emigration at Pacific Grove (where            4. Discussion
limpets were not individually tagged), we restrict our
analysis of limpet mortality to fenced enclosure plots.           Intertidal environments often feature sharp thermal
There was no effect of shading on limpet mortality at          gradients and experience extreme temperature variation,
either site. At Bodega Bay, percentage limpet mortality         by which organism distribution and abundance can be
under shades (mean ± standard error of raw data: 20.9          greatly affected (Newell, 1979). Temperature is also
± 6.6) was statistically similar to mortality in unshaded        known to influence the rates of per capita interactions in
plots (9.6 ± 4.7) (blocked ANOVA, shade effect              the intertidal (Sanford, 1999). As a result of its impacts
F = 1.72, p = 0.238). At Pacific Grove, percentage            on abundance and per capita interaction strength,
mortality in shaded and unshaded plots (9.5 ± 4.5 and          temperature plays a major role in structuring intertidal
4.8 ± 2.2, respectively) was also statistically indistin-        communities (Sanford, 1999; Harley, 2003; Harley and
guishable (blocked ANOVA, shade effect F = 0.47,             Lopez, 2003; Schiel et al., 2004).
p = 0.524).                                 Our experiments were designed to interpret the effects
  In case a shading effect was obscured by among-site         of thermal stress on high-intertidal microalgae, grazing
variation in temperature, we examined the direct effect         limpets, and plant–herbivore interactions. We hypothe-
of temperature on limpet mortality. Rock temperature           sized that increased thermal stress would directly affect
(in the adjacent unfenced plots) had no effect on limpet         limpet feeding rates, growth, and mortality, and both
mortality in limpet inclusion plots at Bodega Bay (linear        directly and indirectly affect microalgal biomass. Unfor-
regression, N = 14, F = 0.36, p = 0.562) or Pacific Grove        tunately, the spring and summer of 2005 did not feature
(linear regression, N = 9, F = 0.81, p = 0.258).             any notable thermal stress events along the Central and
                                     Northern California coastline. Instead, upwelling-related
3.5. Limpet growth                            fog prevailed during this period. Despite the moderate
                                     thermal conditions, our manipulations did create thermal
  Both the intertidal height (F1,25 = 7.8386; R2adj. =         differences between treatments, and our results indicate
0.388; p = 0.0097) and the initial length of the limpets         that temperature is an important factor in our study system.
170      B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173


4.1. Temperature and bottom-up effects               massive mortality of this limpet (Sutherland, 1970).
                                  Second, in the absence of severe stress, warmer
  Both macroalgae and microalgae are susceptible to        temperatures tend to favor L. scabra growth (Gilman,
thermal stress (Matta and Chapman, 1995; Blanchard         2006b). Contrary to these previous findings, tempera-
et al. 1997). Although we found no evidence of thermal       ture had no measurable effect on L. scabra growth or
effects on macroalgae, there were distinct differences       mortality during our experiment. The lack of mortality is
among shading treatments in terms of microalgal           not surprising, given the lack of severe thermal stress.
chlorophyll. Benthic microalgal production is strongly       Rock temperatures at Bodega Bay in the spring of 2004,
influenced by temperature (Grant, 1986; Migné et al.,        for example, exceeded 40 °C in several areas occupied
2004). In general, benthic microalgal photosynthetic        by L. scabra (Harley, unpublished data). The maximum
rates increase with temperature to an optimum between        temperature we recorded during the spring/summer of
15 °C and 30 °C, depending on the study (Rasmussen         2005 was 38.5 °C. The absence of a temperature effect
et al., 1983; Blanchard et al., 1997). Above this          on limpet growth could result from counteractive
optimum, photosynthetic rates decrease (Rasmussen          thermal effects on the food supply, an offsetting of
et al., 1983; Blanchard et al., 1997). In our experiment,      thermal benefits by sublethal thermal stress, or high
shaded, and thus cooler, treatments contained higher        variability and low sample size.
microalgal chlorophyll than the non-shaded plots at both        L. scabra had a strong, negative effect on microalgal
experimental locations, suggesting that temperatures in       chlorophyll at Pacific Grove but not at Bodega Bay.
unshaded plots (which regularly exceeded 30 °C) were        However, this top-down effect was not influenced by
higher than optimal for microalgal production. If this       temperature (i.e. the shade × limpet interaction term was
trend holds true for future climatic regimes, this could      not significant). L. scabra at Bodega Bay had a weak
lead to a suppression of microalgal production as          but consistent negative effect on macroalgal abundance.
temperatures rise. Epilithic biofilms play a key role in      Although L. scabra is thought to feed only on
marine ecosystems, and they represent the main fraction       microalgae (Sutherland, 1972), it is likely that the
of biomass produced and directly consumed in situ on        microscopic stages of macroalgae are also consumed by
exposed rocky shores (Thompson et al., 2004). Thus, a        L. scabra, which may explain the negative interaction
reduction in the microalgal food supply could have         between the limpet and the development of macroscopic
profound effects on intertidal community structure via       stages. However, as with microalgal suppression at
limitation of herbivore density or growth (e.g. Harley,       Pacific Grove, macroalgal suppression at Bodega Bay
2002; Thompson et al., 2004).                    was independent of temperature.
  Contrary to our expectations, L. scabra growth in our        Although we did not demonstrate a thermal effect on
experiment was not correlated with epibenthic chloro-        rates of herbivory, we cannot rule out a thermally-
phyll. Previous work in Northern California has shown        triggered cascade under more stressful conditions.
that microalgal food supply, as estimated by benthic        Temperature-related L. scabra mortality events have
chlorophyll, is an important determinant of L. scabra        been observed in the past (Sutherland, 1970, Harley
growth, although complex interactions exist between         unpublished data), and thermal stress greater than that
chlorophyll and temperature (Gilman, 2006a). Because        which we observed over the course of our study may
L. scabra grows faster during the winter than during        reduce limpet populations to the point where algal cover
the summer (Sutherland, 1970), it is possible that we did      and abundance would increase in response. The exact
not record a growth signal due to very low summer          nature of such a cascade would depend on the relative
growth rates. However, there was a significant relation-      resistance and resilience of producer and consumer
ship between growth and intertidal height (see below),       populations during and following a thermal stress event.
which indicates that growth differences are measurable       In our study, the absence of temperature-related limpet
even during the summer. Our results suggest that some        mortality precluded the development of such density-
other factor, such as available foraging time or sublethal     mediated indirect effects.
stress, limited L. scabra growth during our experiment
(see below).                            4.3. Shore-level effects

4.2. Temperature and top-down effects                 L. scabra living lower on the shore grew faster than
                                  conspecifics living higher up, which agrees with
  Temperature has been shown to influence L. scabra        previous results from this site during the late spring/
in two ways. First, extreme thermal stress results in        early summer (Sutherland, 1970). Sutherland (1970)
        B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173    171


also showed that limpet populations higher in the          shades to experimentally decrease temperature. Al-
intertidal exhibited more seasonal growth rates, which       though shading is a highly effective way to manipulate
presumably resulted from externally induced changes in       organismal temperature at low tide (Harley and Lopez,
food availability. Indeed, microalgal production          2003), shades have very little if any influence on body
decreases, and the seasonality of production increases,       temperature at high tide due to the rapid transfer of heat
with increasing shore level (Nicotri, 1977). Although it      between organisms and moving water. Our results are
is tempting to conclude that higher limpet growth rates       thus specific to the effects of temperature during low
at lower shore levels in our study are attributable to       tide (i.e. atmospheric warming) but not at high tide (i.e.
higher primary production, we found no link between         oceanic warming). The high-intertidal community
limpet growth and indicators of micro- or macroalgal        studied here is underwater for a relatively small
productivity. Alternatively, lower shore animals may        proportion of the time, suggesting that air temperature
have avoided some of the energetic costs of sub-cellular      may be more biologically relevant than water temper-
thermal protection and repair functions (e.g. Somero,        ature; water temperature is more closely tied to limpet
2002). However, we found no relationship between          body temperatures in the low intertidal zone (Denny
limpet growth and average daily maximum temperature.        et al., 2006). Nevertheless, previous research has shown
Limpets at lower shore levels may simply have had          that both air and water temperatures influence the
more time available for foraging, and growth may thus        success of grazing intertidal invertebrates (Gilman,
be limited by foraging time rather than by thermal stress      2006a), suggesting that plant–herbivore interactions
or the availability of algal biomass. It is also possible      may depend on temperature during both emersion and
that patterns in limpet growth rates are complicated by       immersion.
spatial variation in intraspecific competition (Suther-         Our experiment was conducted during the spring and
land, 1970).                            summer, when high temperature stress was most likely
                                  to be important. We therefore cannot shed any light on
4.4. Differences between locations                 the ecological significance of thermal changes during
                                  the winter. Much of the warming in California over the
  Bodega Bay and Pacific Grove were generally           past half century has been an increase in winter
similar in their thermal environments during the course       minimum temperatures (Nemani et al., 2001). Like the
of our study. However, the importance of limpets varied       effects of increased sea surface temperature, winter
between sites; limpets suppressed macro- but not          warming is unlikely to exceed the thermal tolerance of
microalgae at Bodega Bay, whereas the reverse was          intertidal species. However, like warming water tem-
true at Pacific Grove. This may be related to the          perature, changes in winter temperatures could impact
differences in the algal assemblage between the two         other aspects of organismal performance such as
locations, i.e. Bodega Bay featured a diverse macroalgal      metabolic rate, growth, and reproduction.
assemblage while Pacific Grove lacked macroalgae at           Finally, our experimental shades may have had
our study sites. Thus, the diet of L. scabra may vary        unintended ecological effects stemming from alteration
between locations, depending on the local availability of      of the light environment. The shade design used here
small macroalgal life stages. Additionally, limpet         reduces light levels by approximately 60–65% (Harley,
density was higher at Pacific Grove (11.6 per plot vs.       2002). Therefore, it is possible that algae in unshaded
7.4 per plot at Bodega Bay), suggesting that density-        plots were subject to damaging UV radiation and/or
mediated processes could be important in the suppres-        photoinhibition while algae in shaded plots were not.
sion of microalgae (see, e.g., Ruesink, 1998). Given that      High-intertidal macroalgae appear to be highly tolerant
L. scabra density declines dramatically north of Bodega       to UV radiation (Gómez et al., 2004). Although
Bay (Gilman, 2005), it is likely that their impacts as       photoinhibition at solar noon is common in intertidal
herbivores also decline with increasing latitude.          macroalgae, most species recover rapidly in the
                                  afternoon and regain full photosynthetic capacity
4.5. Caveats                            (Gómez et al., 2004). In a heroic experiment which
                                  simultaneously manipulated light, temperature, and
  Applying our results to the issue of climate change       desiccation, Matta and Chapman (1995) found interac-
requires several caveats regarding the timing and          tive effects of temperature and desiccation on photo-
method of thermal manipulation. Owing to the difficulty       synthetic performance of an emersed intertidal brown
of experimentally increasing temperatures in the          alga (Colpomenia perigrina), but no effect of light
intertidal zone, we were constrained to use artificial       intensity. This evidence, along with the lack of a shading
172      B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173


effect on macroalgae in our study, suggests that light did     via interspecific interactions to other members of the
not play a large role as a confounding variable with        community.
regards to macroalgal cover in our experiment.
  It is also possible that UV damage and photoinhibi-       Acknowledgements
tion influenced the microalgae in our experiment.
Although artificially elevated levels of UV radiation         We thank the Bodega Marine Laboratory, University
can negatively impact benthic microalgae on mudflats,        of California — Davis, and the Hopkins Marine Station,
ambient levels of UV radiation have no significant         Stanford University, for providing lab facilities and
effects on benthic microalgal chlorophyll a concentra-       access to field sites. Particular thanks are due to S.L.
tions (Sundbäck et al., 1996; Underwood et al., 1999).       Williams, who provided access to the chlorophyll
Photoinhibition has been documented in the micro-          analysis equipment. Thanks to M. Bracken, A. Car-
phytobenthos following long exposures to very high         ranza, M. Engelbrecht, K. Mach, L. Miller, B. Miner, J.
irradiance (Blanchard et al., 2004); however, several        O'Riley, J. Shinen, and J. Sones for advice and
field studies failed to find evidence for photoinhibition      assistance. This manuscript benefited from comments
in temperate zone sand- and mudflat microflora           by R. Roijackers, M. Bracken, and two anonymous
(Rasmussen et al., 1983; Grant, 1986; Barranguet          reviewers. This research was supported by a Schure-
et al., 1998; Migné et al., 2004). Furthermore, in studies     Beijerinck-Popping Fund grant to B. Morelissen, and
that have simultaneously examined the effects of          Bodega Marine Laboratory institutional funds to C.D.G.
irradiance and temperature on benthic microalgae,          Harley. This is contribution #2381 of the Bodega
thermal effects tend to explain most of the variation in      Marine Laboratory. [SS]
photosynthetic parameters (Rasmussen et al., 1983;
Grant, 1986; Migné et al., 2004). Given these results,       References
plus the fact that temperatures in our unshaded plots
                                  Allison, G., 2004. The influence of species diversity and stress
exceeded optimal temperatures for benthic microalgal
                                    intensity on community resistance and resilience. Ecol. Monogr.
production (see, e.g., Blanchard et al., 1997), it seems        74, 117–134.
reasonable to assume that temperature was more           Bakun, A., 1990. Global climate change and intensification of coastal
important than irradiance in driving benthic chlorophyll        upwelling. Science 247, 198–201.
patterns in our experiment. However, we are not aware        Barranguet, C., Kromkamp, J., Peene, J., 1998. Factors controlling
of controlled manipulations of both light and tempera-         primary production and photosynthetic characteristics of intertidal
                                    microphytobenthos. Mar. Ecol. Prog. Ser. 173, 117–126.
ture with regards to epilithic microphytobenthos, and        Blanchard, G.F., Guarini, J.-M., Gros, P., Richard, P., 1997. Seasonal
the exact determination of the relative importance of          effect on the relationship between the photosynthetic capacity of
temperature and light in driving microalgal production         intertidal microphytobenthos and temperature. J. Phycol. 33,
on hard substrata awaits further experimentation.            723–728.
                                  Blanchard, G.F., Guarini, J.-M., Dang, C., Richard, P., 2004.
                                    Characterizing and quantifying photoinhibition in intertidal
4.6. Conclusions                            microphytobenthos. J. Phycol. 40, 692–696.
                                  Branch, G.M., 1981. The biology of limpets: physical factors, energy
  In intertidal systems, there is a strong potential for       flow, and ecological interactions. Oceanogr. Mar. Biol. Annu. Rev.
temperature to disproportionately impact populations at         19, 235–380.
                                  Connor, V.M., Quinn, J.F., 1984. Stimulation of food species growth
different trophic levels and thus alter bottom-up and top-
                                    by limpet mucus. Science 225, 843–844.
down interactions (Sanford, 1999; Harley, 2003; Harley       Cubit, J.D., 1984. Herbivory and the seasonal abundance of algae on a
and Lopez, 2003). In the present study, we found that          high intertidal rocky shore. Ecology 65, 1904–1917.
microalgae were indeed more susceptible to thermal         Dahlhoff, E.P., Buckley, B.A., Menge, B.A., 2001. Physiology of the
stress than were herbivorous limpets. However, thermal         rocky intertidal predator Nucella ostrina along an environmental
impacts on microalgae did not propagate up the food           stress gradient. Ecology 82, 2816–2829.
                                  Denny, M.W., Harley, C.D.G., 2006. Hot limpets: predicting body
chain to indirectly influence L. scabra. Furthermore,          temperature in a conductance-mediated thermal system. J. Exp.
although limpets had exerted strong top-down control of         Biol. 209, 2409–2419.
specific algal functional groups at specific locations, the     Denny, M.W., Miller, L.P., Harley, C.D.G., 2006. Thermal stress on
strength of top-down control did not change with            intertidal limpets: long-term hindcasts and lethal limits. J. Exp.
temperature. Our results suggest that changes in thermal        Biol. 209, 2420–2431.
                                  Gilman, S.E., 2005. A test of Brown's principle in the intertidal limpet
stress, such as those accompanying climate change, may         Collisella scabra (Gould, 1846). J. Biogeogr. 32, 1583–1589.
disproportionately affect specific trophic levels, but       Gilman, S.E., 2006a. Life at the edge: an experimental study of a
that these direct impacts will not necessarily propagate        poleward range boundary. Oecologia 148, 270–279.
          B. Morelissen, C.D.G. Harley / Journal of Experimental Marine Biology and Ecology 348 (2007) 162–173             173


Gilman, S.E., 2006b. The northern geographic range limit of the         macroalga Colpomenia peregrina Sauv. (Hamel). J. Exp. Mar.
  intertidal limpet Collisella scabra: a test of performance,         Biol. Ecol. 189, 13–27.
  recruitment, and temperature hypotheses. Ecography 29, 709–720.      Migné, A., Spilmont, N., Davoult, D., 2004. In situ measurements of
Gilman, S.E., 2007. Shell microstructure of the patellid gastropod        benthic primary production during emersion: seasonal variations
  Collisella scabra (Gould): ecological and phylogenetic implica-       and annual production in the Bay of Somme (eastern English
  tions. Veliger 48, 235–242.                         Channel, France). Cont. Shelf Res. 24, 1437–1449.
Gómez, I., López-Figueroa, F., Ulloa, N., Morales, V., Lovengreen, C.,    Nemani, R.R., White, M.A., Cayan, D.R., Jones, G.V., Running, S.W.,
  Huovinen, P., Hess, S., 2004. Patterns of photosynthesis in 18        Coughlan, J.C., Peterson, D.L., 2001. Asymmetric warming over
  species of intertidal macroalgae from southern Chile. Mar. Ecol.       coastal California and its impact on the premium wine industry.
  Prog. Ser. 270, 103–116.                           Clim. Res. 19, 25–34.
Grant, J., 1986. Sensitivity of benthic community respiration and       Newell, R.C., 1979. Biology of Intertidal Animals. Marine Ecological
  primary production to changes in temperature and light. Mar. Biol.      Surveys Ltd., Faversham, Kent.
  90, 299–306.                               Nicotri, M.E., 1977. Grazing effects of four marine intertidal
Harley, C.D.G., 2002. Light availability indirectly limits herbivore       herbivores on the microflora. Ecology 58, 1020–1032.
  growth and abundance in a high rocky intertidal community during     Nielsen, K.J., 2001. Bottom-up and top-down forces in tide pools: test
  the winter. Limnol. Oceanogr. 47, 1217–1222.                 of a food chain model in an intertidal community. Ecol. Monogr.
Harley, C.D.G., 2003. Abiotic stress and herbivory interact to set range     71, 187–217.
  limits across a two-dimensional stress gradient. Ecology 84,       Rasmussen, M.B., Henriksen, K., Jensen, A., 1983. Possible causes of
  1477–1488.                                  temporal fluctuations in primary production of the microphyto-
Harley, C.D.G., Helmuth, B.S.T., 2003. Local- and regional-scale         benthos in the Danish Wadden Sea. Mar. Biol. 73, 109–114.
  effects of wave exposure, thermal stress, and absolute vs. effective   Ruesink, J.L., 1998. Variation in per capita interaction strength:
  shore level on patterns of intertidal zonation. Limnol. Oceanogr.      thresholds due to nonlinear dynamics and nonequilibrium condi-
  48, 1498–1508.                                tions. Proc. Natl. Acad. Sci. U. S. A. 95, 6843–6847.
Harley, C.D.G., Lopez, J.P., 2003. The natural history, thermal        Sagarin, R.D., Barry, J.P., Gilman, S.E., Baxter, C.H., 1999. Climate-
  physiology, and ecological impacts of intertidal mesopredators,       related change in an intertidal community over short and long time
  Oedoparena spp. (Diptera: Dryomyzidae). Invertebr. Biol. 122,        scales. Ecol. Monogr. 69, 465–490.
  61–73.                                  Sanford, E., 1999. Regulation of keystone predation by small changes
Harley, C.D.G., Hughes, A.R., Hultgren, K.M., Miner, B.G., Sorte, C.J.B.,    in ocean temperature. Science 283, 2095–2097.
  Thornber, C.S., Rodriguez, L.F., Tomanek, L., Williams, S.L., 2006.    Schiel, D.R., Steinbeck, J.R., Foster, M.S., 2004. Ten years of induced
  The impacts of climate change in coastal marine systems. Ecol. Lett. 9,   ocean warming causes comprehensive changes in marine benthic
  228–241.                                   communities. Ecology 85, 1833–1839.
Haven, S.B., 1973. Competition for food between the intertidal        Sept, J.D., 2002. The Beachcomber's Guide to Seashore Life of
  gastropods Acmaea scabra and Acmaea digitalis. Ecology 54,          California. Harbour publishing, Canada. 312 pp.
  143–151.                                 Sommer, F., 1982. Biological studies on upper intertidal and splash
Hayworth, A.M., Quinn, J.F., 1990. Temperature of limpets in the         zone organisms. Hopkins Marine Station Student Report.
  rocky intertidal zone: effects of caging and substratum. Limnol.     Somero, G.N., 2002. Thermal physiology and vertical zonation of
  Oceanogr. 35, 967–970.                            intertidal animals: optima, limits, and costs of living. Integ. Comp.
Helmuth, B.S.T., Hofmann, G.E., 2001. Microhabitats, thermal           Biol. 42, 780–789.
  heterogeneity, and patterns of physiological stress in the rocky     Sundbäck, K., Nilsson, C., Odmark, S., Wulff, A., 1996. Does ambient
  intertidal zone. Biol. Bull. 201, 374–384.                  UV-B radiation influence marine diatom-dominated microbial
Helmuth, B., Harley, C.D.G., Halpin, P.M., O'Donnell, M., Hofmann, G.E.,     mats? A case study. Aquat. Microb. Ecol. 11, 151–159.
  Blanchette, C.A., 2002. Climate change and latitudinal patterns of    Sutherland, J.P., 1970. Dynamics of high and low populations of the
  intertidal thermal stress. Science 298, 1015–1017.              limpet, Acmaea scabra (Gould). Ecol. Monogr. 40, 169–188.
Hiscock, K., Southward, A., Tittley, I., Hawkins, S., 2004. Effects of    Sutherland, J.P., 1972. Energetics of high and low populations of the
  changing temperature on benthic marine life in Britain and Ireland.     limpet, Acmaea scabra (Gould). Ecology 53, 430–437.
  Aquat. Conserv.: Mar Freshw Ecosyst. 14, 333–362.             Thompson, R.C., Norton, T.A., Hawkins, S.J., 2004. Physical stress
IPCC, 2001. Climate change 2001: synthesis report. A Contribution of       and biological control regulate the producer–consumer balance in
  Working Groups I, II, and III to the Third Assessment Report of the     intertidal biofilms. Ecology 85, 1372–1382.
  Intergovernmental Panel on Climate Change. Cambridge Univer-       Underwood, G.J.C., Nilsson, C., Sundbäck, K., Wulff, A., 1999.
  sity Press, Cambridge, U.K.                         Short-term effects of UV-B radiation on chlorophyll fluorescence,
Jessee, W.F., 1968. Studies of homing behavior in the limpet Acmaea       biomass, pigments, and carbohydrate fractions in a benthic diatom
  scabra. Veliger 11 (52–55).                         mat. J. Phycol. 35, 656–666.
Keser, M., Swenarton, J.T., Foertch, J.F., 2005. Effects of thermal      Welschmeyer, N.A., 1994. Fluorometric analysis of chlorophyll a in
  input and climate change on growth of Ascophyllum nodosum          the presence of chlorophyll b and pheopigments. Limnol.
  (Fucales, Phaeophyceae) in eastern Long Island Sound (USA).         Oceanogr. 39, 1985–1992.
  J. Sea Res. 54, 211–220.                         Wolcott, T.G., 1973. Physiological ecology and intertidal zonation in
Leonard, G.H., 2000. Latitudinal variation in species interactions: a test    limpets (Acmaea): a critical look at “limiting factors”. Biol. Bull.
  in the New England rocky intertidal zone. Ecology 81, 1015–1030.       145, 389–422.
Matta, J.L., Chapman, D.J., 1995. Effects of light, temperature and
  desiccation on the net emersed productivity of the intertidal